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Extreme Physiological Plasticity in a Hibernating Basoendothermic Mammal, Tenrec Ecaudatus Michael D

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Extreme Physiological Plasticity in a Hibernating Basoendothermic Mammal, Tenrec Ecaudatus Michael D © 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb185900. doi:10.1242/jeb.185900 RESEARCH ARTICLE Extreme physiological plasticity in a hibernating basoendothermic mammal, Tenrec ecaudatus Michael D. Treat1,*, Lori Scholer1, Brandon Barrett1, Artur Khachatryan1, Austin J. McKenna1, Tabitha Reyes1, Alhan Rezazadeh1, Charles F. Ronkon1, Dan Samora1, Jeremy F. Santamaria1, Claudia Silva Rubio1, Evan Sutherland1, Jeffrey Richardson2, John R. B. Lighton2 and Frank van Breukelen1,* ABSTRACT hypothetical placental ancestor Schrëwdinger. Schrëwdinger was Physiological plasticity allows organisms to respond to diverse presumed to lack a cloaca, but to have a large and gyrencephalic conditions. However, can being too plastic actually be detrimental? brain, zygomatic arches and tympanic bullae, and internal testes ’ Malagasy common tenrecs, Tenrec ecaudatus,havemany (O Leary et al., 2013). In comparison, tenrecs have a cloaca and, in plesiomorphic traits and may represent a basal placental mammal. the case of Tenrec ecaudatus, have the smallest brain relative to We established a laboratory population of T. ecaudatus and found body mass of all extant mammals (including monotremes and extreme plasticity in thermoregulation and metabolism, a novel marsupials), are lissencephalic, lack zygomatic arches and tympanic hibernation form, variable annual timing, and remarkable growth and bullae, and have internal testes that are located near the kidneys (Lillegraven and Eisenberg, 1983). These features would suggest reproductive biology. For instance, tenrec body temperature (Tb)may approximate ambient temperature to as low as 12°C even when that tenrecs may be reminiscent of basal placental mammals. In Lovegrove’s (2012) plesiomorphic–apomorphic endothermy tenrecs are fully active. Conversely, tenrecs can hibernate with Tb of 28°C. During the active season, oxygen consumption may vary 25-fold model, he posited that ancestral mammals were heterothermic and more rigid homeothermy is a derived condition. Lovegrove (2012) with little or no change in Tb. During the austral winter, tenrecs are consistently torpid but the depth of torpor may vary. A righting assay defines a basoendotherm simply as any mammal with a body temperature (Tb) in the 20th percentile of the frequency distribution revealed that Tb contributes to but does not dictate activity status. Homeostatic processes are not always linked, e.g. a hibernating tenrec of the mammalian Tb dataset, meaning they must exhibit resting Tb experienced a ∼34% decrease in heart rate while maintaining constant <35°C. Lovegrove (2012) notes that the endothermic conditions of body temperature and oxygen consumption rates. Tenrec growth rates extant basoendotherms were likely also exhibited by Cretaceous or vary but young may grow ∼40-fold in the 5 weeks until weaning and early Cenozoic mammals. Tenrecs are considered basoendothermic may possess indeterminate growth as adults. Despite all of this because of the presumed phylogenetic placement of afrotherians profound plasticity, tenrecs are surprisingly intolerant of extremes in and because existing data suggest their Tb is generally <35°C ambient temperature (<8 or >34°C). We contend that while plasticity (Lovegrove, 2012). Tb is also moderately variable in many of the may confer numerous energetic advantages in consistently moderate basal mammalian taxa; some monotremes, marsupials, xenarthrans environments, environmental extremes may have limited the success and afrotherians experience active Tb that varies by as much as 8°C and distribution of plastic basal mammals. (Schmidt-Nielsen et al., 1966; McManus, 1969; Scholl, 1974; Gilmore et al., 2000; Oelkrug et al., 2012). The limited existing data KEY WORDS: Thermoregulation, Oxygen consumption, Variable on active tenrecs suggest a Tb always <35°C with moderate variation body temperature (Tb=31.82±0.098°C, mean±s.e.m.; Racey and Stephenson, 1996; Poppitt et al., 1994; Lovegrove et al., 2014, Levesque and INTRODUCTION Lovegrove, 2014; Levesque et al., 2014). Tenrecs are basoendothermic placental mammals primarily from More pronounced heterothermy in small mammals occurs during Madagascar that are phylogenetically placed in Afrotheria hibernation in conjunction with metabolic depression. Importantly, (Lovegrove, 2012; Everson et al., 2016). Prevailing thought is that metabolic depression and low Tb are linked, e.g. it is thought that a small tenrec species arrived in Madagascar 30–56 MYA and the metabolic depression allows Tb to decrease and that the low Tb radiated into the remaining extant species (Poux et al., 2008; may allow depression of metabolic processes (e.g. van Breukelen and Everson et al., 2016). This tremendous adaptive radiation resulted in Martin, 2015). For instance, hibernating ground squirrels experience species that are terrestrial, fossorial, arboreal and even aquatic decreases of Tb to as low as −2.9°C (Barnes, 1989) and oxygen (Garbutt, 1999). Tenrecs have many ‘ancestral’ features that seem consumption rates to as low as 1/100th of active rates. Hibernation even more plesiomorphic than those of the reconstructed is also found in basal mammals including the echidna, some marsupials, and afrotherians like the elephant shrew, golden moles and tenrecs (Ruf and Geiser, 2015; Scantlebury et al., 2008). All five 1School of Life Sciences, University of Nevada, Las Vegas, Las Vegas, NV 89154, spiny tenrec species, including the focus of this work, T. ecaudatus, USA. 2Sable Systems International, Las Vegas, NV 89032, USA. are known to hibernate (Stephenson and Racey, 1994). The limited *Authors for correspondence ([email protected]; data on hibernating T. ecaudatus demonstrate that Tb follows soil [email protected]) temperature for the duration of the hibernation season with no evidence of brief periods of euthermy between bouts of torpor M.D.T., 0000-0002-3247-4601; L.S., 0000-0002-7596-2058; T.R., 0000-0001- 7128-6366; D.S., 0000-0001-7452-8922; F.v.B., 0000-0001-9653-0273 (Lovegrove et al., 2014). The lack of interbout arousals is unique for small hibernators. Interestingly, dwarf lemurs (Cheirogaleus medius) Received 6 June 2018; Accepted 20 August 2018 will arouse from hibernation if they experience significant periods Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2018) 221, jeb185900. doi:10.1242/jeb.185900 wherein ambient temperature (T ) is <30°C (Dausmann et al., 2004; Respirometry a ̇ Dausmann et al., 2005). Soil temperature in the T. ecaudatus field Aerobic respirometry (oxygen consumption, VO2, and carbon ∼ ̇ study was as low as 22°C for several months. An interesting dioxide production, VCO2) was measured with the Promethion question is whether T. ecaudatus would arouse if hibernating at an Continuous Metabolic Phenotyping System and ExpeData even lower Ta or whether these tenrecs simply hibernate continuously. software (Sable Systems International, Las Vegas, NV, USA). The If tenrecs are indeed plesiomorphic, perhaps a lack of interbout Promethion system auto-baselines for 30 s every 15 min with arousal was an ancestral hibernation characteristic. If so, what may be environmental air, otherwise sampling from each metabolic gleaned from characterizing the physiology of tenrec hibernation? chamber every second. Metabolic chambers were constructed from We established a breeding colony of T. ecaudatus in order to Lettuce and Produce Keeper containers (∼1.8 l; Container Store, examine key parameters affecting their life history in the controlled Coppell, TX, USA). Flow rates were 500 ml min−1. Preliminary setting of the laboratory. We found captive tenrecs to exhibit analyses revealed tenrecs to display three physiological states: extreme physiological plasticity. Active and hibernating tenrecs hibernation, facultative torpor and active. During the austral winter, may have identical Tb. Numerous other tenrec life history traits are tenrecs were hibernating and showed the typical signs of torpor, e.g. also highly plastic. We question why such a plastic mammal is not Tb approached Ta and tenrecs were lethargic even when disturbed. more successful, i.e. if being plastic has selective advantages, then We noted that upon entry into the metabolic chamber, Tb would why do the tenrecs not have a more robust global distribution? We sometimes slowly increase by 1–6°C for various periods (taking up provide a surprising explanation that being too plastic may have to 3–4 h to peak with a similar period to return to the original value) limited the success and distribution of such mammals in more in what appeared to be a partial thermal arousal. Importantly, these variable environments. Moreover, by being more precise in their tenrecs maintained a lethargic state typical of torpor and never thermoregulation and physiology, the more modern boreoeutherian aroused to an active state. Furthermore, at Ta <20°C, tenrecs were mammals may have evolved to persist in more variable noted to experience 30–45 min apneic periods. To avoid sampling environments, leading to a wider global distribution. bias caused by the partial thermal arousals and the apneic periods, data for hibernating tenrecs represent an 8 h period of stable Tb (after MATERIALS AND METHODS ∼14 h of a typical 24 h assay). During the active season (after the Acquisition and maintenance of the T. ecaudatus colony resumption of feeding, i.e. October to April), tenrecs were also Forty wild-caught common tenrecs, T. ecaudatus (Schreber 1778),
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